Functional multimodality of axonal tree in invertebrate neurons

This review, based on invertebrate neuron examples, aims at highlighting the functional consequences of axonal tree organization. The axonal organization of invertebrate neurons is very complex both morphologically and physiologically. The first part shows how the transfer of information along sensory axons is modified by presynaptic inhibition mechanisms. In primary afferents, presynaptic inhibition is involved in: 1) increasing the dynamic range of the sensory response; 2) processing the sensory information such as increasing spatial and/or temporal selectivity; 3) discriminating environmental information from sensory activities generated by the animal's own movement; and 4) modulating the gain of negative feedback (resistance reflex) during active rhythmic movements such as locomotion. In a second part, the whole organization of other types of neurons is considered, and evidence is given that a neuron may not work as a unit, but rather as a mosaic of disconnected 'integrate-and-fire' units. Examples of invertebrate neurons are presented in which several spike initiating zones exist, such as in some stomatogastric neurons. The separation of a neuron into two functionally distinct entities may be almost total with distinct arborizations existing in different ganglia. However, this functional separation is not definitive and depends on the state of the neuron. In conclusion, the classical integrate-and-fire representation of the neuron, with its dendritic arborization, its spike initiating zone, its axon and axonal tree seems to be no more applicable to invertebrate neurons. A better knowledge of the function of vertebrate neurons would probably demonstrate that it is the case for a large number of them, as suggested by the complex architecture of some reticular interneurons in vertebrates.